The Myth of Monogamy: Fidelity and Infidelity in Animals and People (17 page)

In the preceding examples, if the females' goal was to increase the genetic diversity of their offspring, then all females should be equally inclined to EPCs. On the other hand, if increasing genetic
quality
or attractiveness is the goal, then females mated with particularly low-quality males should be especially EPC-prone (which they are). If there are only a few good males--and especially if these are very good--then EPCs should be particularly frequent. By contrast, if all males are pretty much so-so, EPCs would offer less genetic payoff. We can also predict that EPCs should be less frequent on islands-- where genetic diversity is low--than on mainlands, where it is high. Similarly for populations that have recently gone through a genetic "bottleneck," resulting in less genetic diversity: Free-living cheetahs, for example, are notoriously inbred and lacking in genetic diversity; it seems likely that female cheetahs are not especially inclined to multiple mating or susceptible to EPCs.

Evolution often works in strange and unexpected ways. This is certainly true when it comes to female preference for particular male traits. Thus, in addition to possibly preferring males who make enough sperm and who carry genes that are suitably varied, complementary, health-related, and sexy, there is good reason to think that females may even favor certain males based on characteristics of their sperm alone.

After all, not all sperm are created equal. Those from different males differ in the likelihood that they will succeed in fertilizing an egg. Studies have been conducted in which a wide range of animals--insects, chickens, mice, rabbits, pigs, cattle--were inseminated with similar amounts of sperm from two or three males. The findings are that, in nearly every case, sperm from a particular male are far more effective than those of other males. There are many reasons for this: Sperm come in different shapes and sizes and with different metabolisms, swimming abilities, and chemical characteristics--all of which can influence sperm motility, longevity, ability to penetrate the egg, ability to survive within the female genital tract, and so forth.

undermining the myth: females (choosing male genes)
81

Since males differ in their capacity to fertilize eggs, it is quite reasonable that females would set up situations that exaggerate these differences. Why? Because it would benefit females to be fertilized by high-fertilizing males, since their own male offspring would then be likely to be high-fertilizers themselves. (We have already encountered the "sexy son hypothesis." Now, meet its close relative, the "sexy sperm hypothesis.")

The simplest way for females to ensure that they are fertilized by sperm that are sexy--or, at least, successful in sperm-sperm competition--is for the females to set up competitions; that is, to mate with more than one male. And this is precisely what many females do. Columbian ground squirrel females, for example, are in estrus for only about four hours per year, yet during this brief window of sexual opportunity, female ground squirrels are very busy, copulating with an average of 4.4 males. In another species of ground squirrel, females are in estrus for less than seven hours per year, and yet during this period, they copulate with an average of 6 to 7 males. And there is no reason to think that ground squirrel females are especially sexually profligate: Even when monogamy is not at issue, multiple mating by females is widespread, and sperm competition may well be the major reason.

But the story is far from over. If females profit by staging sperm competition, it stands to reason that they would profit even more if they could make the competition especially intense by creating a genital environment that is challenging and difficult, not only consisting of many different participants but also outfitted with obstacles both mechanical and physiological. For example, by extending the length of one's genital tract, the swimming capacity of sperm is highlighted. Insects and spiders are especially notorious for having tortuous reproductive systems, a series of lengthy gauntlets through which sperm must swim. May the best man-- rather, the best sperm--win. (The resulting pattern has been called "cryptic female choice," something likely to be especially important in cases when females have relatively little opportunity for choosing a mating partner more overtly.)

Incidentally, there is nothing unique about females setting high standards for would-be suitors: defend a territory, engage in suitable (and often difficult) courtship rituals, provide lots of food during and after courtship, win a jousting tournament, slay a dragon, swim the Hellespont, and so forth. Consider, for example, that chimpanzee females commonly mate with many different males. It is probably no coincidence that male chimpanzees, in addition to sporting exceptionally large testicles (enabling them to produce large quantities of sperm), also have long penises. A longer penis almost certainly gives its possessor's sperm an advantage, since they could be deposited

82
THE MYTH OF MONOGAMY

closer to the cervix. This, in turn, would be especially significant if sperm from more than one male are competing within a female, which of course is precisely what happens if the female mates with multiple males while she is ovulating. (And this is exactly what female chimps do.)

In one study, detailed measurements of 11 males and 19 females showed that in 10 of the 11 males, penis length actually exceeded the vaginal depth of 14 of the 19 females! This is not as strange as it might appear, since the length of a chimpanzee's vagina varies with her menstrual cycle, becoming maximum when the pink sexual skin is maximally swollen, which is also at the time of ovulation. Among some females, vaginal length increases during ovulation by as much as 50 percent. As a result, 7 of the 11 males described above would have been unable to reach the cervix of
any
of the 19 females, while the remaining 4 would only be capable of reaching some of them. By increasing the length of their vaginas when they ovulate, female chimpanzees make it more difficult for males to fertilize them, giving an advantage to sexual partners who produce sperm that are especially abundant, mobile, capable of withstanding the rigors of the vaginal environment, and delivered by a long penis. (Is this
why
the vaginas of ovulating chimps grow longer? Good question.)

Strangely enough, among all species practicing internal fertilization, it is virtually unknown for the male to introduce his sperm directly upon the female's eggs, which would result in immediate fertilization. Always the eggs are kept back, deeper inside, while the sperm are deposited in some sort of antechamber, from which they must proceed along various twisty canals, sluiceways, and storage containers, often lined with cilia (which not uncommonly beat in the opposite direction), traversing what--for a tiny sperm-- must seem like hundreds of miles, generally through rather inhospitable terrain, chemically debilitating if not outright lethal, and, as if that were not enough, frequently patrolled by comparatively huge and aggressive sperm-eating phagocytes.

In an article titled "Why Do Females Make It So Difficult for Males to Fertilize Their Eggs?", biologists Tim Birkhead, Anders Miller, and W.J. Sutherland emphasized that "in terms of its structure, chemical composition and immune response, the female reproductive tract of mammals and birds is particularly hostile to sperm" and that, as a result, females are likely to be fertilized by the fittest sperm or, at least, to minimize the risk that they will be fertilized by the "worst." Imagine that males differ in their ability to overcome such female hostility. A female who indiscriminately allows any male to fertilize her eggs is likely to produce sons who themselves will only be able to fertilize a small subset of the females in their generation. By contrast, by setting up a difficult and demanding obstacle course, a female makes it likely that her sons will be able to fertilize most females.

undermining the myth: females (choosing male genes)
83

If it were in the interests of females to make fertilization easy, it would not require much of a stretch in evolutionary potential to imagine a very different situation, in which sperm were ejaculated onto--or, at worst, very near--the eggs they were "intended" to fertilize. But although it is assuredly in the interests of females for fertilization to occur (just as it is in the interest of males), there is very little reason for females to make it easy. Indeed, there are good reasons to make it difficult. Or rather, one good reason: sperm competition.

"The phrase sperm competition," according to entomologist and evolutionary theorist William Eberhard, "evokes the image of armies of tiny, one-tailed soldiers racing up female ducts, or struggling in hand-to-hand combat to gain access to large, passive treasures. It emphasizes, as has been traditional in biology, the active male role in male-female interactions."

But in fact, as Eberhard points out, females may well hold the key to victory in sperm competition:

Simple, relatively insignificant movements of the female, such as a few "downstream" peristaltic twitches of her reproductive tract, or beating in the wrong direction of the cilia lining the reproductive tract, can result in the army of little "warriors" being unceremoniously dumped from her body, or being diverted to other internal sites where they will be digested.

Responding, in all likelihood, to female maneuvering, male insects, for example, engage in a wide array of peculiar antics during copulation. William Eberhard, one last time: "Males of different insect species lick, tap, rub, push, kick, stroke, shake, squeeze, feed, sing to, and vibrate the female during copulation." All this, it seems, in an effort to overcome the female's resistance.

Females set up numerous barriers to fertilization; for example, the vaginas of most mammals have a very low pH, which is detrimental to the survival of sperm. The traditional explanation for an acidic vagina is that it reduces the danger of microbial infection. Supposedly, therefore, females do what they have to do--that is, acidify their reproductive tracts--to protect themselves, leaving sperm to cope however they can. Once females have opted to lower their vaginal pH, males must attempt to deliver sperm that will make the best of their difficult situation. With lots of sperm being produced, at least some have a good chance of making it. (And after all, any males that elected to opt out of the competition would be truly left out, supplanted by those that took the plunge, however acidic.)

At the same time--and here is the new twist--females are free to lower their pH even more, giving rise to additional male-male competition,

84
the myth of monogamy

resulting perhaps in acid-resistant, armored gladiatorial sperm whose voyaging capacity might rival that of Marco Polo, seminal secretions that temporarily increase pH, and so forth. Either way, females could in this manner end up using their low vaginal pH as a kind of sperm-screening device.

The female reproductive tract is notoriously unfriendly to sperm in other respects. Not uncommonly, the cervix is home to millions of leukocytes (white blood cells) that in other contexts devour bacterial invaders but that have quite an appetite for invading sperm as well; after all, sperm, too, are foreign to the female's body. Among human beings in particular, there are also high concentrations of antisperm antibodies in the cervical mucus. And to make things harder yet, female reproductive anatomy is typically elaborate, with eggs reachable only after sperm have completed a lengthy, twisty, and difficult upstream migration. Even then, sperm do not typically receive a warm hero's welcome: Eggs themselves are often stubbornly difficult to penetrate.

The effectiveness of these various antisperm defenses is attested by the fact that only a minute proportion of the vast numbers of sperm introduced into a female even get near her eggs. Until recently, this has widely been seen as due to the vagaries of chance, but the point is that it may not be a matter of chance at all; rather, antifertilization barriers may be specifically erected by females. It would be especially interesting to see if species characterized by a high level of EPCs turn out to be those in which female reproductive tracts are especially tortuous or possess a high level of antisperm antibodies, a particularly low vaginal pH, eggs that are unusually difficult to penetrate, and so forth.

At the same time, researchers must beware a tendency to overinterpret the mating advantages enjoyed by certain males over others, seeing any such imbalance as evidence that females are necessarily promoting sperm competition when they might not be doing anything of the sort. For example, it was found that when female dungflies copulate with large and small males, the former fertilize the lion's share of the eggs. Tempting as it is to attribute this to active selection by females of the sperm of large males, it turns out that this large-male advantage is simply due to the fact that large males transfer sperm at a higher rate. Nonetheless, it seems increasingly clear that in many cases--perhaps most--females are active participants in their own fertilization, not just in the choice of whom they mate with but also regarding what happens afterward.

If a female has only one sexual partner, there is no payoff for her in making things difficult for him. But if she mates with several males, it would probably be in a female's interest for her eggs to be "hard to get"-- guarded, like Sleeping Beauty, by dragons, impenetrable thornbushes, and

undermining the myth: females (choosing male genes)
85

other daunting barriers. The successful Prince Charming should be not only charming, but also persevering and capable of producing sperm that are equally so.